ResearchArticle Brucella Seroprevalence in a High-Risk...

Research ArticleBrucella Seroprevalence in a High-Risk Population in Greece:A Cross-Sectional Study

Panagiotis Andriopoulos ,1 Dimitrios Floros,1 Natalia Gioti,1 AnargirosMariolis,2

Andrea Paola Rojas Gil,3 andMaria Tsironi 1

1Laboratory of Epidemiology and Prevention of Hemoglobinopathies, Acute and Chronic Diseases, Department of Nursing,University of Peloponnese, Valioti & Plateon, 23100 Sparta, Laconia, Greece2Areopoli Health Center, Areopoli 23062, Laconia, Greece3Laboratory of Biology and Biochemistry, Department of Nursing, University of Peloponnese, Valioti & Plateon,23100 Sparta, Laconia, Greece

Correspondence should be addressed to Panagiotis Andriopoulos; [email protected]

Received 11 September 2018; Revised 29 November 2018; Accepted 5 December 2018; Published 25 December 2018

Academic Editor: Alex Grinberg

Copyright © 2018 Panagiotis Andriopoulos et al.This is an open access article distributed under theCreative Commons AttributionLicense,whichpermits unrestricteduse, distribution, and reproduction in anymedium, provided the original work is properly cited.

Introduction. Brucellosis is a zoonosis with high occupational risk. However, seroprevalence of Brucella antibodies amongoccupational groups is not known, since studies in endemic countries are rare. Methods. A cross-sectional seroprevalence studywas conducted among livestock farmers in an endemic region in Greece. A low-risk group of individuals that just moved in theregionwas used as controls. Rose Bengal,Wright standard tube agglutination (STA) tests, and specific IgG and IgMantibodies usingELISA were evaluated; differences and odds ratioswere calculated. Results were comparedwith studies fromother endemic regions.Results. 100 livestock farmers and family members and 34 first-year students were enrolled. Rose Bengal results were 18% positiveversus 0% (p=0.007); Wright STAs for Brucella melitensis were 8% versus 2.9% (p=0.448) and for Brucella abortus they were 2%versus 2.9% (p=0.588). ELISA IgGwas positive in 8%of farmers versus 2.9% of students (p=0.448). Parallel testingwith Rose Bengaland ELISA IgG was positive in 3% versus 0% (p=0.571). No significant odds ratios were calculated forWright STAs and ELISA IgG.Conclusions. Healthy livestock farmers may present with positive Rose Bengal test but this translates to true seroprevalence in onlya small proportion. Livestock farmers have no significant seroprevalence that may obscure diagnosis of acute brucellosis in clinicalsettings.

1. Introduction

Brucellosis remains the most common zoonosis worldwide[1]. Despite the eradication efforts, reports from all over theworld reveal the burden of the disease in not only well-known endemic countries [2–5] but also in countries wherebrucellosis was not a major health problem until recently [6–8]. Brucellosis is a disease with occupational interest, since agreat percentage of the affected population is livestock farm-ers, their families, slaughterhouse workers, and veterinarians[9–12]. Infection in occupational settings occurs throughdirect contact from cuts and skin abrasions, inhalation ofcontaminated aerosols, and contactwith conjunctivalmucosaand of course by consuming contaminated dairy products[13, 14].

Brucellosis has been a major health problem in Greece.Many reports from different parts of the country point to theneed for a continuous surveillance system [10, 13–17]. Mostof them have identified occupational exposure and residencein rural areas as common risk factors for the development ofinfection. Diagnosis of brucellosis in these reports is mainlybased on isolation of Brucella spp. Even though isolationof the pathogen by culture of body fluids is consideredthe gold standard [18], fast and reliable serological testsprovide results rapidly and are also used for diagnosis [19,20]. Enzyme-linked immunosorbent assay (ELISA) tests areanother alternative, both in clinical settings and in prevalencestudies. Individual specific IgG and IgM immunoglobulinscan be measured rapidly but at a much greater cost thansimple agglutination tests [21].

HindawiInterdisciplinary Perspectives on Infectious DiseasesVolume 2018, Article ID 8751921, 6 pageshttps://doi.org/10.1155/2018/8751921

http://orcid.org/0000-0003-0368-4973http://orcid.org/0000-0002-0569-6217https://creativecommons.org/licenses/by/4.0/https://creativecommons.org/licenses/by/4.0/https://doi.org/10.1155/2018/8751921

2 Interdisciplinary Perspectives on Infectious Diseases

Seroprevalence ofBrucella antigens has been documentedin studies from endemic areas in Asia [22–24], Sub-SaharanAfrica [25, 26], and Turkey [27]. Seroprevalence studies fromEurope are limited. Reports on serological tests are limitedto diagnostic procedures on patients [28] or on follow-upof former patients [19]. Aim of this study is to evaluate theseroprevalence of Brucella antigens in a high-risk populationof an endemic region in Europe and compare the results withlow-risk individuals from the same area.

2. Materials and Methods

Laconia is a mostly rural area located in Peloponnese, south-ern Greece. Brucellosis is a common health problem andhas been described elsewhere [10, 13, 15]. Livestock farmers(mainly flocks of sheep and goats) are scattered all over thestate. Healthy participants from the official state databasewere randomly selected. A short questionnaire on possibleacute infection during the past 6 months was completedincluding information on fever, malaise, arthralgias, low backpain, headache, and other common clinical symptoms ofbrucellosis. Blood samples were obtained in order to performserology tests. Cluster sampling had been performed and, forevery consenting professional, family sampling was sought.In total, 100 different individuals from 57 sampling sitesparticipated in the study. Sampling was performed fromOctober 2015 to September 2016.

In order to compare serology results from high- andlow-risk populations, we asked first-year students of ourDepartment of Nursing in Sparta to participate in the study.Students were eligible to take part in the study if they hadcome from urban areas from other parts of Greece exceptPeloponnese and had no family occupational history thatmight have led to contact with Brucella spp. and no history ofpast infection.They also completed the same questionnaire asthe livestock farmers. The recruitment was completed within1 month of residency in Laconia in two parts, newcomers ofSeptember 2015 and of September 2016. From all candidates,34 were randomly selected. We did not include any otherlower-risk individuals that had a permanent residency inour state in the control group because we decided to havedifferent population person and place characteristics in termsof descriptive epidemiology.

Serological evaluation was performed using Brucellaagglutination tests: the Rose Bengal slide agglutination test(RB) and the Wright standard tube agglutination (STA) testwith reagents by LinearChemicals S.L.U. Rose Bengal antigenis a suspension of Brucella abortus colored with Rose Bengalstain. For our study, blood sampling was taken by venipunc-ture, and the serum was separated from each sample aftercentrifuging. Sera were stored and divided into aliquots at−20∘C until use. For RB, 0.05 ml of serum was mixed with anequal volume of antigen on a test plate to produce a zone thatis approximately 2 cm in diameter. In ambient temperatureafter agitation, the mix was observed for agglutination andany visible reaction was considered positive. No dilutionswere performed for Rose Bengal test. All sera were routinelytested with STA both in low and in high dilutions (from 1/40to 1/1600) in order to avoid negative results due to prozone

phenomenon. STA was performed by adding 0.05 ml ofabortus andmelitensis antigens in low- and high-diluted sera.The dilutions were observed for agglutination after gentleagitation. Agglutination in any dilution was considered aspositive result. Brucella abortus antibodies were measured byELISAusingMPBiomedicalsGermanyGmbH’sBrucella IgMELISA and Brucella IgG ELISA kits. Results higher than 50U/ml and 40 U/ml accordingly were considered positive.

Statistical analysis of the data was conducted using theSPSS v23 and STATA 14.0 packages. Descriptive statistics(frequencies, means, and 95% confidence intervals (CI)) weremeasured for each test. Differences in categorical variableswere evaluated by Fisher’s exact test for small samples.Differences in means were evaluated with Student’s t-test.In this cross-sectional study, odds ratios (ORs) with 95%confidence intervals (95%CI) and p values were calculated toestimate the probability of positive results in the two groups ofparticipants. Results were considered statistically significantwhen p < 0.05.

Written informed consent was obtained from all par-ticipating individuals. Blood sampling was performed aftercompleting the questionnaires and all safety precautionswere undertaken. The study was approved by the Universityof Peloponnese’s ethics committee in accordance with theethical standards laid down by the 1964 Declaration ofHelsinki and its later amendments.

3. Results

100 livestock farmers and family members and 34 studentsof the Nursing Department participated in the study. Figure 1depicts the geographical distribution of the 19 sites (villages)where cluster sampling was performed. Serological results aresummarized in Table 1.The occupationally exposed high-riskpopulation was, as expected, older than the group of students(mean age 57.7 years (95% CI 54.31-60.97) versus 19.5 years(95% CI 19.23 – 19.58)) and predominantly male. 18% of thehigh-risk group had positive Rose Bengal test, 8% Wrightmelitensis STA, and 2% abortus STA (positive results in RoseBengal test in all patients with positive STA tests; however,some of them had positive STA for melitensis and otherstested positive for STA abortus). The students had no positiveRose Bengal and only one tested positive for both STA tests.The difference between groups was significant only for RoseBengal (p=0.007).

ELISA serology tests provided different results. No posi-tive values of the test were recorded in the high-risk group forIgM antibodies (mean IgM for livestock farmers 4.33 U/ml(95% CI 2.37 – 6.28)). Two students had positive IgM anti-bodies in the absence of positive agglutination tests and thiswas considered to be randomerror.No statistically significantdifferences were recorded in titers of IgG antibodies (meanof livestock farmers 7.96 U/ml (95% CI 3.11 – 12.8) versus4.06 U/ml (95%CI 0.52 – 7.59)) of students (p=0.367). Thedifference in positive results was also not significant: 8% inthe high risk versus 2.9% in low risk (p=0.448). Only 3% ofthe livestock farmers had both Rose Bengal and ELISA IgGpositive and none of the students had that (p=0.571).

Interdisciplinary Perspectives on Infectious Diseases 3

Table 1: Serology results in high- and low-risk populations.

Livestock farmers Students p valueAge 57.7 (54.31 – 60.97) 19.5 (19.52 – 19.58)


Table 2: Odds ratio for positive test in high- versus low-risk population.

Odds ratio 95% confidence interval P valueRose Bengal -Wright abortus 0.67 (0.05 – 7.74) 0.75Wrightmelitensis 2.87 (0.34 – 24.21) 0.31ELISA IgM -ELISA IgG 2.87 (0.34 – 24.21) 0.31Odds ratios were calculated if possible. In ratios with no positive results, no ORs could be calculated.

predominantly or occasionally in close contact with theanimals [10, 16].

Serological agglutination tests are used for rapid diagno-sis of brucellosis worldwide. Several studies have evaluatedtheir sensitivity and specificity on patients and healthyindividuals [20, 31, 32] with various results but, as shownelsewhere [19], these results have to take into account theprevalence of the disease in order to provide accurate infor-mation. Diaz et al. [20] have suggested titration and dilutionfor the RB test but this procedure is not regularly reportedin the literature. Wright STA tests are considered positivein dilutions equal to or greater than 1/160; some researcherseven suggest 1/320 in endemic areas. In a large case seriesof acute brucellosis [13], we found that no such thresholdis safe, since many patients had culture-proven brucellosiswith positive results only in 1/80 dilutions. In our study,we documented a difference between STAs for abortus andmelitensis in livestock farmers.Thismight be explained by thepredominance of sheep and goats in the flocks, but this is onlya hypothesis.

IgM and IgG antibodies have been used for diagnosis ofbrucellosis for decades; however, commercial kits in regularpractice have been widely available in the past decade.Various studies have evaluated their performance [31–33, 36].Most studies focus on the reliability of the essays to diagnosechronic and relapsing cases. In acute brucellosis, the resultsare usually the same with serology. However, in developingcountries and rural areas where the disease is highly endemic,ELISA antibodies are rarely used on seroprevalence studiesand the prevalence of IgG antibodies among high-risk pop-ulations is not regularly reported. In our study, the positiveRB test was not confirmed by ELISA and the probabilityof having a positive result of IgG antibodies in livestockfarmers as calculated byORswas also not significantly higher.This difference between serology and ELISA confirms aprevious report that estimated the positive prognostic valueof serology tests for brucellosis to only 11.4% [19]. Two ofthe low-risk individuals (5.9%) had a positive IgM ELISAtest without any symptoms or signs of the disease. This is aconfirmation of a well-discussed problem in brucellosis thatno laboratory result can provide diagnosis in the absence ofclinical and epidemiological data that point to the disease[5, 20, 28].

A MEDLINE/Google Scholar search was performedusing keywords Brucella/brucellosis and seroprevalence,brucellosis seroprevalence, and high risk occupation. The

majority of the studies focused on seroprevalence as adiagnostic procedure in order to identify patients. The aimof our study was to measure seroprevalence of brucellosis inhealthy individuals, so we compared our results only withstudies that had such information. Moreover, we selectedreports from livestock farmers and not veterinarians orabattoir workers, since the exposure risk is not the same. Intotal, we found only 11 studies that fulfilled our criteria. InTable 3, the results from our study are compared with otherrelevant reports from endemic areas. In our study, 18% of thehigh-risk population had positive RB and 8% positive IgGantibodies and Wright STA was positive in 2% for abortusand 8% for melitensis antigens. Studies from different areas,the Mediterranean Basin [27, 31, 33], sub-Saharan Africa [12,25, 26], the Middle East [34, 35], and Asia [22–24], providea different serological profile in high-risk populations and inhealthy individuals where available. The tests used tomeasureseroprevalence differ in each study, but overall positive RBranges from 2% to 18.6% and ELISA IgG from 2.86% to 16.7%(either ELISA IgG or ELISA IgG and agglutination tests).7 out of 11 studies reported results only from agglutinationtests.

Several limitations are present in our study. First, live-stock farmers from only one region of Greece were studiedand the disease is endemic in the whole country. Second,implications can bemade for only one high-risk occupationalgroup and not veterinarians or abattoir workers. Finally,dilutions in the Rose Bengal test were not performed andthis might explain the relatively high positive results in thistest.

5. Conclusions

In conclusion, we performed a seroprevalence study ofbrucellosis in a high-risk occupational group and comparedit with a low-risk population. We found minimal differencesfor positive results in Wright STA tests and in ELISAIgG antibodies and a significant difference in Rose Bengaltest, a difference that was minimized when RB and ELISAIgG were combined. To our knowledge, this is the onlyseroprevalence study of brucellosis in healthy individualsin an endemic area from Europe and it points to the factthat livestock farmers have no significant seroprevalence thatmay obscure diagnosis of acute brucellosis in clinical set-tings.

Interdisciplinary Perspectives on Infectious Diseases 5

Table 3: Comparative results of seroprevalence studies in endemic areas.

RB Wright STA ELISA G ELISA M Parallel testing StudyMediterranean

Greece (100) 18% 8% (M) 8% 0% 3%1

Turkey (573) 11.9% 5.4% (N/A) Vancelik et al [27]Spain (90)2 0% 0% (A) 0% 0% Gomez et al [28]Turkey (528) 4% 5.2% (N/A) Kose et al. [33]

AfricaAngola (132) 16.7%3 Mufinda et al. [12]Tanzania (67) 2% Swai et. al. [25]Uganda (140) 18.6% Tumwine et al.[26]

Middle EastIran (292) 5.5 % (N/A) NIkokar et al [34]Iran (250)4 6.4% (N/A) Esmaeli et al.[35]

AsiaMongolia (2856) 11.1% Tsend et al. [22]India (121)5 9.91% 9.09% (N/A) 16.52% Sharma et al. [23]Bangladesh (386) 2.86%6 Rahman et al [24]

Results from seroprevalence studies in livestock farmers. In each study, the number of subjects is mentioned after the country. The study from Spain (Gomezet al.) is included because it provides the only other available seroprevalence data from Europe we identified in our literature search. In STA tests, M denotesmelitensis, A denotes abortus, and N/A denotes being not mentioned.1RB and ELISA IgG.2Healthy blood donors.3Positive STA and ELISA.4 5All high-risk groups.6Positive RB, STA, and ELISA.

Data Availability

The SPSS and STATA files with the data used to support thefindings of this study are available from the correspondingauthor.

Conflicts of Interest

There are no conflicts of interest to declare.

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